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1 Department of Radiology, Osaka University Graduate School of Medicine, 2-2
Yamadaoka, Suita, Osaka, 565-0871, Japan.
2 Department of Radiology, National Kinki Chuo Hospital for Chest Disease, 1180
Nagasone-cho, Sakai, Osaka, 591-8025, Japan.
3 First Department of Internal Medicine, Kumamoto University School of Medicine,
1-1-1 Honjo, Kumamoto, 860-0811, Japan.
4 Department of Radiology, Kurume University School of Medicine, 67 Asahi-machi,
Kurume, 830-0011, Japan.
5 First Department of Internal Medicine, Kurume University School of Medicine,
Kurume, 830-0011, Japan.
6 Department of Radiology, Hokkaido University School of Medicine, North-15,
West-7, Kita-Ku, Sapporo, 060-8638, Japan.
7 Department of Radiology, University of British Columbia and Vancouver Hospital
and Health Sciences Center, 855 W. 12th Ave., Vancouver, B. C. V5Z 1M9,
Canada.
Received July 10, 2002;
accepted after revision August 27, 2002.
Address correspondence to M. Koyama.
Abstract
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MATERIALS AND METHODS. High-resolution CT scans in 92 patients with chronic cystic lung diseases (18 with pulmonary Langerhans cell histiocytosis, 18 with pulmonary lymphangioleiomyomatosis, 17 with usual interstitial pneumonia, 16 with lymphocytic interstitial pneumonia, 15 with emphysema, and eight with desquamative interstitial pneumonia or respiratory bronchiolitis interstitial lung disease) were retrospectively assessed by two independent observers without knowledge of the clinical or pathologic data. The observers recorded the abnormalities, the most likely diagnosis, and the degree of confidence in that diagnosis.
RESULTS. The two observers made a correct first-choice diagnosis in 148 (80%) of 184 interpretations. The correct diagnosis was made in 100% of interpretations of usual interstitial pneumonia, 81% of desquamative interstitial pneumonia or respiratory bronchiolitis interstitial lung disease, 81% of lymphocytic interstitial pneumonia, 77% of emphysema, 72% of lymphangioleiomyomatosis, and 72% of Langerhans cell histiocytosis. The two observers made a diagnosis with a high degree of confidence in 105 (57%) of 184 interpretations. The confident diagnosis was correct in 98 (93%) of 105 interpretations.
CONCLUSION. Although various chronic cystic lung diseases often have a characteristic appearance that allows their distinction on high-resolution CT, considerable overlap exists among the CT findings. Therefore, lung biopsy is often required for a definitive diagnosis.
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Histologic diagnosis was made on the basis of specimens obtained at open lung or video-assisted thoracoscopic lung biopsy in all patients with usual interstitial pneumonia, desquamative interstitial pneumonia or respiratory bronchiolitis interstitial lung disease, Langerhans cell histiocytosis, and lymphangioleiomyomatosis, and in ten patients with lymphocytic interstitial pneumonia, and at transbronchial lung biopsy in six patients with lymphocytic interstitial pneumonia. In three patients with emphysema, the diagnosis was confirmed by the analysis of the surgical specimen from lung-volume reduction surgery; in the remaining 12 patients with emphysema, the diagnosis was made on the basis of clinical, functional, and radiographic criteria. Four (25%) of 16 patients with lymphocytic interstitial pneumonia, two (11%) of 18 patients with lymphangioleiomyomatosis, and all (100%) patients with usual interstitial pneumonia, desquamative interstitial pneumonia or respiratory bronchiolitis interstitial lung disease, emphysema, and Langerhans cell histiocytosis were current or former smokers.
All patients underwent high-resolution CT of the chest. The CT scans consisted of 1- to 3-mm collimation sections reconstructed with a high-spatial-frequency algorithm. The protocols consisted of thin sections obtained at 1-cm intervals (59 patients), 1.5-cm intervals (21 patients), or 2-cm intervals (12 patients). All CT scans were obtained at end inspiration using a variety of scanners and with the patient in the supine position. No IV contrast material was used. All CT scans were performed before the specific diagnosis of each disease, and none of patients was receiving any treatment at the time of high-resolution CT.
The CT scans were randomized and then reviewed separately by two independent chest radiologists who were unaware of any clinical or histologic findings other than the age and sex of the patient. The observers were aware that only six types of cystic lung diseases were included in the study, but they did not know the frequency of the entities.
The high-resolution CT scans were assessed for the presence, extent, and
anatomic distribution of areas of ground-glass attenuation, areas of air-space
consolidation, intralobular reticular opacity, interlobular septal thickening,
thickening of bronchovascular bundles, bronchial wall thickening,
bronchiectasis, traction bronchiectasis, emphysema, honeycombing,
centrilobular branching structures, and nodules. Nodules were divided into
three sizes: small nodules (short axis diameter < 1 cm), large nodules (1-3
cm), and masses (>3 cm). Associated abnormalities, including
lymphadenopathy and pleural effusions, were also assessed. Lymphadenopathy was
considered present when the short axis diameter of the nodes was greater than
1 cm. The cross-sectional distribution was classified as central if there was
a predominance of abnormalities in the inner third of the lung, peripheral if
there was a predominance of abnormalities in the outer third of the lung, and
random if there was no predominance. Predominant distribution in the
cephalocaudal axis was classified as upper lung zone predominance, lower lung
zone predominance, or random. Upper lung zone predominance was considered
present when most of the abnormalities were situated above the level of the
tracheal carina; lower lung zone predominance, when most of the abnormalities
were located below this level; and random distribution, when involvement of
the upper and lower lung zones was equivalent. In addition, the observers
recorded the following findings for each patient: cyst configuration (round or
lobulated), size of cysts (small, <1 cm; medium, 1-2 cm; large, >2 cm),
cyst wall appearance (not identified; thin, 
1 mm; thick, >1 mm), extent
of cysts (clustered or scattered), parenchymal abnormalities around cysts
(consolidation or ground-glass attenuation), and distribution of cysts (upper,
lower, or random). The cysts were classified as clustered if there was contact
between them (Fig. 1) and as
scattered if there was no contact between them.
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CT findings were interpreted on the basis of previously published data [7, 8, 14,15,16,17,18,19,20,21,22] about the CT appearance of these six diseases. Subsequently, each observer recorded the most likely diagnosis for each patient and graded their degree of confidence in their diagnosis as high (level 1) or low (level 2). Interobserver variability was assessed using kappa statistics [28]. Kappa values larger than zero were considered to indicate a positive correlation; values up to 0.20 were considered positive but showing poor agreement; values of 0.21-0.40, fair agreement; values of 0.41-0.60, moderate agreement; values of 0.61-0.80, good agreement; and values greater than 0.81, excellent agreement. The mean number of correct diagnoses and the mean number of CT findings for the two observers were tabulated.
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The two observers made a correct first-choice diagnosis with a high degree
of confidence in 53% of cases. The confident diagnosis (average of two
observers) was correct in all cases (100%) of usual interstitial pneumonia,
88% of cases of desquamative interstitial pneumonia or respiratory
bronchiolitis interstitial lung disease, 94% of cases of lymphocytic
interstitial pneumonia, 100% of cases of emphysema, 88% of cases of
lymphangioleiomyomatosis, and 88% of cases of Langerhans cell histiocytosis
(Table 1). Agreement between
the observers was fair for the correct diagnosis (
= 0.33) and for the
correct diagnosis with a high degree of confidence ( = 0.22).
The frequencies of various CT findings are summarized in Table 2. Areas of ground-glass attenuation were found in all patients with usual interstitial pneumonia, desquamative interstitial pneumonia or respiratory bronchiolitis interstitial lung disease, and lymphocytic interstitial pneumonia (Figs. 1,2,3), and less commonly in the other diseases (Fisher's exact probability test; p < 0.005). Centrilobular branching structures were present in 56% of the interpretations of lymphocytic interstitial pneumonia, in 50% of the interpretations of Langerhans cell histiocytosis, and less commonly in the other diseases (Fisher's exact probability test; p < 0.01). Intralobular reticular opacities were seen in 50% of the interpretations of desquamative interstitial pneumonia or respiratory bronchiolitis interstitial lung disease, in 32% of the interpretations of usual interstitial pneumonia, and less commonly in the other diseases (Fisher's exact probability test; p < 0.05). Thickening of bronchovascular bundles was identified in 59% of the interpretations of lymphocytic interstitial pneumonia (Fig. 3) and less commonly in the other diseases (Fisher's exact probability test; p < 0.001). Traction bronchiectasis was common in usual interstitial pneumonia (88% of the interpretations) (Fig. 1) and less common in the other entities (Fisher's exact probability test; p < 0.0001). None of the patients with emphysema or Langerhans cell histiocytosis had pleural effusion or lymphadenopathy.
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Upper lung zone predominance of the abnormalities was seen in 67% of the interpretations of Langerhans cell histiocytosis (Fig. 4) and less commonly in the other diseases (Fisher's exact probability test; p < 0.05). Lower lung zone predominance was identified in 94% of the interpretations of usual interstitial pneumonia (Fig. 1), in 75% of the interpretations of desquamative interstitial pneumonia or respiratory bronchiolitis interstitial lung disease (Fig. 2), and less commonly in the other diseases (Fisher's exact probability test; p < 0.005). A predominantly peripheral distribution was seen in 100% of interpretations of usual interstitial pneumonia and less commonly in the other diseases (Fisher's exact probability test; p < 0.05). Lymphangioleiomyomatosis (Fig. 5) and lymphocytic interstitial pneumonia frequently showed random distribution in both the cephalocaudad and the cross-sectional planes.
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The frequencies of characteristic CT findings of the cyst appearance in each disease are summarized in Table 3. Large (> 2 cm diameter) cysts were found in 70% of the interpretations of emphysema (Fig. 6) and less commonly in the other diseases (Fisher's exact probability test; p < 0.05). Clustered cysts were found in 100% of the interpretations of usual interstitial pneumonia (Fig. 1) and less commonly in the other diseases (Fisher's exact probability test; p < 0.01). Lower lung zone predominance of cysts was found in 97% of the interpretations of usual interstitial pneumonia and less commonly in the other diseases (Fisher's exact probability test; p < 0.0001). Cysts arising in the areas of ground-glass attenuation were seen in 88% of the interpretations of desquamative interstitial pneumonia or respiratory bronchiolitis interstitial lung disease (Fig. 2), in 76% of the interpretations of usual interstitial pneumonia (Fig. 1), and less commonly in the other diseases (Fisher's exact probability test; p < 0.05).
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Frequencies of characteristic combinations of CT findings are summarized in Table 4. A combination of traction bronchiectasis, clustered distribution of cysts, and lower zone predominance of cysts was prominent in usual interstitial pneumonia (85% of the interpretations) (Fig. 1) and was seen less commonly in the other diseases (Fisher's exact probability test; p < 0.0001). A combination of areas of ground-glass attenuation around the cysts and no perceptible cyst wall was identified in 56% of the interpretations of desquamative interstitial pneumonia or respiratory bronchiolitis interstitial lung disease (Fig. 2) and was less common in the other diseases (Fisher's exact probability test; p < 0.01). A combination of interlobular septal thickening, thickening of bronchovascular bundles, and scattered distribution of cysts was found in 53% of the interpretations of lymphocytic interstitial pneumonia (Fisher's exact probability test; p < 0.001).
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The incorrect diagnoses in each disease made by each observer are summarized as follows. Observer 2 misdiagnosed four cases of lymphocytic interstitial pneumonia. Langerhans cell histiocytosis was given as the incorrect diagnosis in 75% of these cases. Observer 1 misdiagnosed two cases of emphysema. Langerhans cell histiocytosis was given as the incorrect diagnosis in both cases (100%). Observer 2 misdiagnosed five cases of emphysema. Usual interstitial pneumonia was given as the incorrect diagnosis in two of these cases (40%) and Langerhans cell histiocytosis, in two cases (40%). Observer 1 misdiagnosed five cases of lymphangioleiomyomatosis. Langerhans cell histiocytosis was given as the incorrect diagnosis in all five cases (100%). Observer 2 misdiagnosed five cases of lymphangioleiomyomatosis. Lymphocytic interstitial pneumonia was given as the incorrect diagnosis in four of these cases (80%). Observer 1 misdiagnosed two cases of Langerhans cell histiocytosis. Desquamative interstitial pneumonia or respiratory bronchiolitis interstitial lung disease was given as the incorrect diagnosis in both cases (100%). Observer 2 misdiagnosed eight cases of Langerhans cell histiocytosis. Lymphocytic interstitial pneumonia was given as the incorrect diagnosis in five of these cases (63%).
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Cystic changes in lung parenchyma are commonly seen in patients with desquamative interstitial pneumonia, usually representing areas of emphysema superimposed on the areas of ground-glass attenuation (Fig. 2). Desquamative interstitial pneumonia is characterized by the presence of increased numbers of intraalveolar macrophages, mild inflammation of alveolar septum, and minimal fibrosis [2]. In respiratory bronchiolitis interstitial lung disease, interstitial thickening similar to that seen in desquamative interstitial pneumonia accompanies the air-space changes but the thickening is confined to the peribronchiolar parenchyma [24]. Because of the histologic and clinical similarities between desquamative interstitial pneumonia and respiratory bronchiolitis interstitial lung disease, these two entities represent different ends of a spectrum of the same disease [24]. The predominant high-resolution CT findings of desquamative interstitial pneumonia or respiratory bronchiolitis interstitial lung disease are areas of ground-glass attenuation and centrilobular nodular opacities (Fig. 2) [16, 17]. A subpleural and basal predominance is often present, and reticular opacities may be associated with the areas of ground-glass attenuation. Associated centrilobular emphysema is also commonly present because of smoking. Heyneman et al. [17] reviewed the high-resolution CT findings in 16 patients with desquamative interstitial pneumonia and eight patients with respiratory bronchiolitis interstitial lung disease. All patients with desquamative interstitial pneumonia had extensive areas of ground-glass attenuation, and emphysema was seen in 50% of patients. The predominant abnormalities in patients with respiratory bronchiolitis interstitial lung disease consisted of areas of ground-glass attenuation, seen in 50% of patients, and centrilobular nodules, seen in 38%. Emphysema was seen in 50% of patients [17]. In our study, areas of ground-glass attenuation were seen in all patients, emphysema in 63%, intralobular reticular opacity in 50%, and small nodules in 44%. A combination of lack of a perceptible cyst wall and areas of ground-glass attenuation around the cysts was found in 56% of cases of desquamative interstitial pneumonia or respiratory bronchiolitis interstitial lung disease and less commonly in the other diseases. The results of our study are similar to those of previous reports. Although no significant differences were found between desquamative interstitial pneumonia or respiratory bronchiolitis interstitial lung disease and emphysema regarding the cyst configuration, cyst wall appearance, extent of cyst, and distribution of cysts, areas of ground-glass attenuation in patients with desquamative interstitial pneumonia or respiratory bronchiolitis interstitial lung disease were significantly greater than in patients with emphysema.
Multiple cystic air spaces are typically seen on high-resolution CT in patients with lymphocytic interstitial pneumonia (Fig. 3). In a study by Johkoh et al. [18], cystic air spaces were found in 15 (68%) of 22 patients with lymphocytic interstitial pneumonia. Lymphocytic interstitial pneumonia is a benign lymphoproliferative disorder characterized by a diffuse and interstitial proliferation of small lymphocytes and plasma cells [25]. Ichikawa et al. [3] correlated high-resolution CT findings of lymphocytic interstitial pneumonia with pathologic findings, and those researchers presumed that the mechanism of cystic formation is partial airway obstruction by peribronchiolar cellular infiltration. The predominant high-resolution CT findings consist of diffuse bilateral areas of ground-glass attenuation and poorly defined centrilobular nodules; other common findings include subpleural nodules, thickening of the bronchovascular bundles, cystic air spaces, and patchy areas of ground-glass attenuation. These CT features were also commonly seen in our study. In addition, scattered distribution of cysts was seen in 94% of patients; clustered distribution of cysts was seen in only 22%. A combination of interlobular septal thickening, thickening of bronchovascular bundles, and scattered distribution of cysts was found in 53% of cases of lymphocytic interstitial pneumonia and was less common in the other diseases (Fisher's exact probability test; p < 0.001). These CT findings and characteristic combinations of findings may be helpful in differentiating lymphocytic interstitial pneumonia from other diseases.
Emphysema (Fig. 6) is a condition of the lung characterized by permanent abnormal enlargement of air spaces distal to the terminal bronchiole that is accompanied by the destruction of the bronchiolar walls [4]. Emphysema is usually classified into three main subtypes on the basis of the anatomic distribution of the areas of lung destruction [8]. These subtypes are centrilobular emphysema, panlobular emphysema, and paraseptal emphysema. In most cases of centrilobular emphysema, the areas of low attenuation lack visible walls, although very thin and relatively inconspicuous walls are occasionally seen [8]. Areas of paraseptal emphysema often have visible walls, but the walls are very thin [8]. In our study, 87% of patients with emphysema and 63% of patients with desquamative interstitial pneumonia or respiratory bronchiolitis interstitial lung disease showed lack of a perceptible cyst wall. In contrast, the lack of a perceptible cyst wall was seen in 36% or fewer of the patients with other diseases. Bonelli et al. [23] reported high-resolution CT findings in 10 patients with emphysema. In that study, all patients with emphysema showed the lack of a perceptible cyst wall. Those researchers concluded that the most important distinguishing features were the lack of a perceptible cyst wall and the central location of vascular structures. Differences of subtypes of emphysema between the two studies may account for the discrepancy.
A relatively lower accuracy in diagnosis was observed in the remaining two cystic lung diseases included in this study, with a correct diagnosis in 72% of patients with lymphangioleiomyomatosis and in 72% of patients with Langerhans cell histiocytosis. The pathologic characteristics of lymphangioleiomyomatosis are diffuse cystic changes associated with the proliferation of atypical smooth muscle cells [5, 26, 30]. The pathogenesis of the cyst formation is not clearly established. The predominant high-resolution CT finding in patients with lymphangioleiomyomatosis is multiple thin-walled cysts distributed diffusely throughout the lungs; irregularly shaped cysts are uncommon (Fig. 5) [8, 19, 20]. The lung parenchyma among the cystic air spaces is usually normal. Small nodules are occasionally seen [21, 31], including rare cases of multifocal micronodular pneumocyte hyperplasia associated with lymphangioleiomyomatosis in patients with tuberous sclerosis [32, 33]; but small nodules are not a prominent feature of this disease, as they are with Langerhans cell histiocytosis [8, 19, 20]. Bonelli et al. [23] reported high-resolution CT findings in 10 patients with Langerhans cell histiocytosis and in nine patients with lymphangioleiomyomatosis. In that study, all patients with lymphangioleiomyomatosis lacked nodules in the intervening lung parenchyma, whereas most patients with Langerhans cell histiocytosis had parenchymal nodules. Those researchers concluded that parenchymal nodules are helpful in distinguishing Langerhans cell histiocytosis from lymphangioleiomyomatosis. In our study, lymphangioleiomyomatosis was misdiagnosed as Langerhans cell histiocytosis in five (100%) cases by observer 1 and in one case (20%) by observer 2. The patients with lymphangioleiomyomatosis in our study had a greater percentage of small nodules (89%) than those reported in previous studies. Consequently, it was difficult to distinguish between lymphangioleiomyomatosis and Langerhans cell histiocytosis.
Multiple cystic changes are also typical CT findings in patients with Langerhans cell histiocytosis (Fig. 4). Langerhans cell histiocytosis is an uncommon disease of unknown etiology. In its early stages, Langerhans cell histiocytosis is pathologically characterized by the presence of granulomas containing large numbers of Langerhans cells and eosinophils and resulting in the destruction of lung tissue [34]. In the later stages of the disease, the granulomas are replaced by fibrosis and cysts [27]. The pathogenesis of cyst formation remains to be established. The high-resolution CT findings have been described in a number of previous reports [6,7,8, 22]. The most common abnormalities on high-resolution CT are cysts and nodules. Wall thickness varies from thin and barely perceptible to several millimeters. Although many cysts appear to be round, bizarre cysts or branching cysts were also seen. Upper lobe predominance in the size and numbers of cysts is common [8]. These CT features were also commonly seen in our study, together with additional findings of upper lung zone predominance of the cysts. Upper lung zone predominance of the abnormalities was seen in 67% of the interpretations of Langerhans cell histiocytosis and less commonly in the other diseases. The cyst configuration in Langerhans cell histiocytosis was more likely to be lobulated than in other diseases; however, no significant difference was observed. Other CT findings, including the wall thickness, were not sufficiently characteristic to allow differentiating Langerhans cell histiocytosis from other diseases. However, a combination of small nodules, lobulated cyst configuration, and upper lung zone predominance of the cysts was more prominent in patients with Langerhans cell histiocytosis, seen in 47% of the interpretations, than in those with other diseases.
Distribution of cystic change may help distinguish usual interstitial pneumonia from other cystic lung diseases. In our study, lower zone predominance of the cysts was prominent in usual interstitial pneumonia (97% of the interpretations) and was less commonly seen in the other diseases. Random distribution of cysts was identified in 72% of the interpretations of lymphocytic interstitial pneumonia and in 64% of the interpretations of lymphangioleiomyomatosis. Cyst wall appearance, extent of the cysts, and lung parenchymal abnormalities around the cysts were additional helpful findings. In contrast, cyst configuration itself is not sufficiently characteristic to differentiate a specific disease from other diseases.
Although individual CT findings were sometimes helpful, the overlap in these findings among cystic lung diseases is still considerable; in many cases, each CT finding alone was not useful for discriminating one disease from another. On the basis of the results of our study, we consider that the most helpful finding in distinguishing cystic lung disease is a combination of traction bronchiectasis, clustered distribution of cysts, and lower zone predominance of cysts to diagnose usual interstitial pneumonia; a combination of areas of ground-glass attenuation around the cyst and lack of a perceptible cyst wall to diagnose desquamative interstitial pneumonia or respiratory bronchiolitis interstitial lung disease; a combination of interlobular septal thickening, thickening of bronchovascular bundles, and scattered distribution of cysts to diagnose lymphocytic interstitial pneumonia; a combination of lack of a perceptible cyst wall and lack of areas of ground-glass attenuation to diagnose emphysema; a combination of lack of areas of ground-glass attenuation, scattered distribution of cysts, and random distribution of cysts to diagnose lymphangioleiomyomatosis; and a combination of small nodules, lobulated cyst configuration, and upper lung zone predominance of the cysts to diagnose Langerhans cell histiocytosis. However, the results of our study show that considerable overlap among the CT findings of the various diseases that precludes a confident diagnosis in approximately 50% of cases.
Our study has several limitations. First, the study was retrospective and included a relatively small number of patients and only a few diseases. Second, because no clinical information was given, the observers were at an unrealistic disadvantage. Several entities had distinct clinical presentations and demographic features. Third, the study was biased because in clinical practice the differential diagnosis must include entities other than chronic cystic lung diseases. Furthermore, the study had a selection bias. The number of patients selected in this study did not reflect the frequency of the disease radiologists encounter in daily clinical practice. Fourth, because most cases were biopsy proven, cases with highly characteristic findings might not have undergone biopsy and thus might have been excluded. Therefore, the reported accuracy values may be artificially low. However, the main goal of our study was to determine whether the findings in various cystic lung diseases are sufficiently characteristic to allow their distinction on high-resolution CT. This goal was achieved, we believe, by having the observers review the findings without awareness of the clinical data and by committing to a diagnosis based on data in the literature.
In conclusion, although various cystic lung diseases often have a characteristic appearance that allows their distinction on high-resolution CT, the CT findings overlap considerably. Therefore, lung biopsy is often required for a definitive diagnosis.
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